How Does Sagittal Spinopelvic Alignment of Lumbar Multisegmental Spondylolysis Differ from Monosegmental Spondylolysis?

CLINICAL ARTICLE J Neurosurg Spine 33:211–218, 2020

How does sagittal spinopelvic alignment of lumbar multisegmental spondylolysis differ from monosegmental spondylolysis?

Qing-shuang Zhou, MM,1 Xu Sun, MD,1 Xi Chen, MD,1 Liang Xu, MD,2 Bang-ping Qian, MD,1 Ze-zhang Zhu, MD,1 Bin Wang, MD,1 and Yong Qiu, MD1

1Department of Spine Surgery, Drum Tower Hospital, Clinical College of Nanjing Medical University, Nanjing; and 2Department of Spine Surgery, Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China

OBJECTIVE The aim of this study was to investigate sagittal alignment and compensatory mechanisms in patients with monosegmental spondylolysis (mono_lysis) and multisegmental spondylolysis (multi_lysis). METHODS A total of 453 adult patients treated for symptomatic low-grade spondylolytic spondylolisthesis were retrospectively studied at a single center. Patients were divided into 2 subgroups, the mono_lysis group and the multi_lysis group, based on the number of spondylolysis segments. A total of 158 asymptomatic healthy volunteers were enrolled in this study as the control group. Radiographic parameters measured on standing sagittal radiographs and the ratios of L4–S1 segmental lordosis (SL) to lumbar lordosis (L4–S1 SL/LL) and pelvic tilt to pelvic incidence (PT/PI) were compared between all experimental groups. RESULTS There were 51 patients (11.3%) with a diagnosis of multi_lysis in the spondylolysis group. When compared with the control group, the spondylolysis group exhibited larger PI (p < 0.001), PT (p < 0.001), LL (p < 0.001), and L4–S1 SL (p = 0.025) and a smaller L4–S1 SL/LL ratio (p < 0.001). When analyzing the specific spondylolysis subgroups, there were no significant differences in PI, but the multi_lysis group had a higher L5 incidence (p = 0.004), PT (p = 0.018), and PT/PI ratio (p = 0.039). The multi_lysis group also had a smaller L4–S1 SL/LL ratio (p = 0.012) and greater sagittal vertical axis (p < 0.001). CONCLUSIONS A high-PI spinopelvic pattern was involved in the development of spondylolytic spondylolisthesis, and a larger L5 incidence might be associated with the occurrence of consecutive multi_lysis. Unlike patients with mono_ly- sis, individuals with multi_lysis were characterized by an anterior trunk, insufficiency of L4–S1 SL, and pelvic retroversion. https://thejns.org/doi/abs/10.3171/2020.2.SPINE191415 KEYWORDS spondylolytic spondylolisthesis; multisegment; monosegment; sagittal alignment; lumbar

umbar spondylolysis, sometimes combined with The pathological mechanisms behind lumbar spondy- spondylolisthesis, predominantly occurs at the lum- lolysis are still not fully understood. Spinopelvic align- bosacral monosegment (mono_lysis).1,2 It is rare ment is an important factor in the occurrence and pro- Lbut possible for spondylolysis to be detected at consecu- gression of single-level spondylolytic spondylolisthesis.6,7 tive multiple regions of the lumbar spine (multi_lysis).3,4 Studies have reported that L5–S1 spondylolytic spondylo- Spondylolysis, with or without spondylolisthesis, is usually listhesis is associated with increased pelvic incidence (PI) asymptomatic; however, some patients may present with compared with that observed in a normal population.7,8 As intractable back pain or radicular symptoms.2 If conserva- demonstrated in biomechanical studies, increased PI gen- tive treatment fails, surgical intervention is an effective so- erates higher repetitive stress at the pars interarticularis lution to achieve solid fusion, neurological decompression, and subsequently results in the development of lumbosa- and restoration of lumbar alignment.5 cral spondylolysis.9 The status of the sagittal plane, such

ABBREVIATIONS LDI = lordosis distribution index; LL = lumbar lordosis; L5I = L5 incidence; mono_lysis = monosegmental spondylolysis; multi_lysis = multisegmental spondylolysis; ODI = Oswestry Disability Index; PI = pelvic incidence; PT = pelvic tilt; QOL = quality of life; SA = slip angle; SL = segmental lordosis; SP = slip percentage; SS = sacral slope; SVA = sagittal vertical axis; TK = thoracic kyphosis; VAS = visual analog scale. SUBMITTED November 25, 2019. ACCEPTED February 10, 2020. INCLUDE WHEN CITING Published online April 17, 2020; DOI: 10.3171/2020.2.SPINE191415.

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Unauthenticated | Downloaded 09/29/21 06:05 AM UTC Zhou et al. as insufficient lordosis, pelvic retroversion, and anterior percentage (SP) and slip angle (SA) of the L3–4, L4–5, sagittal malalignment, has been reported to be associated and L5–S1 levels were measured at the spondylolysis and with clinical presentation.10 Analyses of sagittal spinopel- spondylolisthesis levels, respectively. Pelvic parameters, vic alignment in patients with lumbosacral spondylolytic including PI, pelvic tilt (PT), and sacral slope (SS), were spondylolisthesis have led to the development of surgical measured as previously described.20 The PT/PI ratio was algorithms and assessment of treatment outcomes.11,12 In- computed to investigate pelvic retroversion.21,22 Also, pel- adequate restoration of lumbar alignment is reported to be vic balance was determined on the nomogram of PT and related to poor patient-reported outcomes,11,13 mechanical SS measurements, as described by Hresko et al.23 L5 inci- complications,12,13 and adjacent-segment disease.14,15 dence (L5I) was measured from the middle of the femo- Lumbosacral consecutive multi_lysis often requires ral heads to the middle of the sacrum plateau and a line surgical intervention because of potential segmental insta- perpendicular to the upper endplate of L5.24 Lumbar lor- bility. However, to our knowledge, no studies have ana- dosis (LL) was measured from the upper endplate of the lyzed the spinopelvic alignment of multi_lysis, whereas L1 vertebra to the upper endplate of S1. L4–S1 segmental only sporadic case reports in the literature have mentioned lordosis (SL) was measured from the upper endplate of or described such a rare disease.4,16,17 Comprehensive in- L4 to the upper endplate of S1. The lordosis distribution terpretation of the sagittal alignment pattern and com- index (LDI) was defined as the ratio of L4–S1 SL to LL, pensatory mechanisms of sagittal balance are essential allowing greater understanding of lordosis distribution for surgical intervention to correct multi_lysis. The goals as upper- and lower-arc lordoses.12,13 Thoracic kyphosis of this study were to 1) investigate the pattern of sagit- (TK) was measured from the upper endplate of T5 to the tal alignment in spondylolytic spondylolisthesis patients lower endplate of the T12 vertebra. Global sagittal align- (both mono_lysis and multi_lysis) in comparison with ment was assessed by the sagittal vertical axis (SVA; the healthy individuals and 2) illustrate differences of sagit- distance between a plumb line from the center of the C7 tal alignment and compensatory mechanisms in patients vertebral body and posterior superior corner of S1). An diagnosed with mono_lysis versus multi_lysis. unbalanced alignment was characterized by an SVA ≥ 4 cm, following the Scoliosis Research Society–Schwab Methods adult spinal deformity classification.25 Patient Population Quality of Life Patients diagnosed with symptomatic spondylolysis with spondylolisthesis who previously underwent surgi- Preoperative quality-of-life (QOL) questionnaires were cal intervention at our center between January 2007 and administered to patients. The Oswestry Disability Index January 2018 were retrospectively studied. Enrolled pa- (ODI) and visual analog scale (VAS) for leg pain and back tients had to meet the following inclusion criteria: 1) age pain were used to evaluate the QOL. 18 years or older and 2) symptomatic lumbar spondylolysis with at least 1 level of spondylolisthesis (Meyerding’s Statistical Analysis grade I or II). Exclusion criteria preventing a patient from Statistical analyses were performed using IBM SPSS being studied included 1) diagnosis of degenerative spon- (version 20.0, IBM Corp.). The mean and standard devia- dylolisthesis; 2) exhibition of lumbar scoliosis > 10°; and tion were calculated for continuous variables. The inde- 3) a previous history of spinal surgery, trauma, infection, pendent-samples t-test was performed to evaluate the dif- or fracture of the pelvis or lower limbs. All spondyloly- ferences between 2 groups. Differences among 3 groups sis patients were diagnosed by 3D-CT radiography of the were evaluated using one-way ANOVA and chi-square lumbar spine. Spondylolisthesis was defined as a forward tests. We first performed an analysis of the demograph- slip of one vertebral body by at least 5% in relation to the ic data for each experimental group. Next, comparison next most caudal vertebral body on upright neutral lateral 18 analysis of the data obtained from radiological analysis radiography. Patient demographic data, including age, was performed between the control and the spondylolysis sex, BMI, and work status, were recorded. The enrolled groups, and among the control, multi_lysis, and mono_ly- patients with spondylolysis were divided into 2 subgroups: sis groups. Pearson correlations were also performed for the mono_lysis subgroup and the multi_lysis subgroup the multi_lysis group. Lastly, QOL scores were compared (Fig. 1). The mono_lysis group included patients with between the spondylolysis subgroups. A p value < 0.05 monosegmental spondylolytic spondylolisthesis, whereas was considered as statistically significant. the multi_lysis group included patients with multilevel spondylolysis and spondylolisthesis in at least one of the spondylolytic levels. A cohort of healthy adult volunteers Results from the Chinese Han population were recruited into the Patient Demographics control group. All studies were approved by the institu- A total of 158 healthy volunteers and 453 spondyloly- tional review board committee. sis patients were included in this study (Table 1). In the spondylolysis group, 51 patients (11.3%) were found to Radiography Analyses have multiple spondylolysis and were categorized into the Radiographic parameters were measured by 2 senior multi_lysis group. There were no significant differences spinal surgeons using upright radiographs, and the mean observed regarding age, sex, BMI, or work status among values were adapted for the analyses (Fig. 2).7,11,19 Slip the 3 groups.

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FIG. 1. Representative lateral radiographs obtained in a patient with double-level spondylolysis (A), a patient with mono_lysis (B), and a healthy individual (C). A: A 59-year-old female with L4–5 and L5–S1 double-level spondylolysis. PI = 70.6°, PT/PI ratio = 42%, L5I = 57.0°, LL = 45.20°, LDI = 16%, SVA = 92 mm. B: A 52-year-old female with L5–S1 mono_lysis. PI = 56.1°, PT/PI ratio = 30.4%, L5I = 25.7°, LL = 57.4°, LDI = 63%, SVA = 9 mm. C: A 46-year-old healthy individual without back pain. PI = 44.3°, PT/PI ratio = 16%, L5I = 14.1°, LL = 52°, LDI = 74%, SVA = −12 mm.

Spondylolisthesis Parameters S1 level in the multi_lysis group (p = 0.002 and p < 0.001, Spondylolytic spondylolisthesis was observed at L5–S1 respectively). in 295 patients, at L4–5 in 102 patients, and at L3–4 in 5 patients in the mono_lysis group. The most common pa- Sagittal Alignment Assessment thology observed in the multi_lysis group was L4–5 and Compared with the control group, the spondylolysis L5–S1 double-level spondylolysis in 40 patients (78.4%), group exhibited significantly larger PI (p < 0.001), PT (p < followed by L3–4 and L4–5 2-level spondylolysis in 6 pa- 0.001), SS (p < 0.001), PT/PI ratio (p < 0.001), and L5I (p tients (11.8%) and L3–4, L4–5, and L5–S1 3-level spondy- < 0.001) (Fig. 3). Although a significantly higher LL (p < lolysis in 5 patients (9.8%). Spondylolisthesis was detected 0.001) and slightly higher L4–S1 LL (p = 0.025) were de- at a single level in 17 patients (L4–5 in 9 and L5–S1 in 8), tected in the spondylolysis group, the SVA (p = 0.003) was at 2 levels in 32 patients (L4–5 and L5–S1 in 29 and L3–4 positive in comparison with the control group due to sig- and L4–5 in 3), and at 3 levels (L3–4, L4–5, and L5–S1) nificant decreases in TK (p < 0.001) and LDI (p < 0.001). in 2 patients in the multi_lysis group. Sagittal alignment parameter data analyzed by one-way Spondylolisthesis-related parameters are summarized ANOVA among the control, multi_lysis, and mono_lysis in Table 2. Both SP and SA at the L3–4 and L4–5 lev- groups are shown in Table 3. PI and SS were found to be els were found to be similar between the multi_lysis and similar in the multi_lysis and mono_lysis groups. How- mono_lysis groups, but were significantly lower at the L5– ever, a slightly greater PT (18.9° ± 9.0° vs 16.3° ± 7.6°, p

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FIG. 2. Radiological parameters measured on upright radiographs. A: Pelvic parameters: PI, PT, SS, and L5I. B: Slip parameters: slip angle (α), slip percentage (line bc/line ac × 100%). C: Sagittal alignment parameters: L4–S1 segmental lordosis (L4–S1 SL), LL, TK, and SVA.

= 0.018) and PT/PI (32% ± 12% vs 29% ± 10%, p = 0.039) were observed in the multi_lysis versus the mono_lysis were observed in the multi_lysis group. In addition, L5I group. There were no significant differences in TK ob- was significantly greater in the multi_lysis group than in served between the subgroups. the mono_lysis group (30.8° ± 14.8° vs 26.0° ± 11.2°, p = As shown in Table 3, the multi_lysis group had a sig- 0.004). Remarkably, smaller LL (53.4° ± 12.0° vs 57.6° ± nificantly greater SVA than the mono_lysis group (24.0 ± 10.7°, p = 0.005), L4–S1 SL (32.8° ± 13.2° vs 37.2° ± 9.1°, 39.7 mm vs 1.87 ± 35.7 mm, p < 0.001). When compared p = 0.004), and LDI (59% ± 21% vs 64% ± 12%, p = 0.012) with the mono_lysis group, more patients in the multi_ly-

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TABLE 1. Demographic data among the normal group and the 2 TABLE 2. Comparison of mean slipping parameters between the spondylolysis subgroups spondylolysis subgroups Control Multi_Lysis Mono_Lysis p Multi_Lysis Group Mono_Lysis Group p Value Group Group Group Value L3–4 SP (%) 10.0 ± 3.5 10.0 ± 3.6 0.202 Mean age, yrs 47.1 ± 11.3 50.1 ± 10.4 48.0 ± 13.2 0.327 L4–5 SP (%) 23.5 ± 11.0 23.3 ± 10.0 0.915 Mean BMI 23.1 ± 3.7 24.4 ± 5.8 23.6 ± 4.3 0.153 L5–S1 SP (%) 17.9 ± 10.5 23.5 ± 10.4 0.002 Male/female 62/96 15/36 143/259 0.425 L3–4 SA (°) 12.9 ± 2.5 6.7 ± 6.5 0.126 Work status L4–5 SA (°) 8.8 ± 7.8 6.9 ± 5.9 0.125 Full or part time 78 22 218 L5–S1 SA (°) 7.0 ± 9.8 9.9 ± 6.6 <0.001 Retired 34 15 102 0.154 Other 46 14 82 Values are presented as the number of patients unless otherwise indicated. have multi_lysis. However, in a study of Japanese general Mean values are presented as the mean ± SD. individuals by Sakai et al.,4 the incidence of multi_lysis was 0.3% (5 of 2000). One reason for this inconsistency may be because our study is based on a cohort of patients sis group were shown to have an SVA ≥ 4 cm (29.4% vs diagnosed with spondylolytic spondylolisthesis who previ- 13.7%, p = 0.003) and an unbalanced pelvis with high PT/ ously underwent surgical intervention. low SS (54.9% vs 40.8%, p = 0.039; Table 4). PI, which is strongly correlated with PT and other sagit- In the multi_lysis group, PI was positively correlated tal alignment parameters, is one of the most important an- with PT (r = 0.668, p < 0.001), SS (r = 0.641, p < 0.001), atomical parameters in the sagittal plane. As demonstrat- L5I (r = 0.745, p < 0.001), LL (r = 0.337, p = 0.016), and ed in biomechanical studies, PI may be associated with the PT/PI ratio (r = 0.358, p = 0.010). In the same group, PI development of spondylolysis as well as the progression of was negatively correlated with LDI (r = −0.426, p = 0.002) spondylolisthesis.7,9 PI was once thought to be greater in (Table 5). There were also positive correlations between patients with multiple spondylolysis. In a study including L5I and PT (r = 0.860, p < 0.001), PT/PI ratio (r = 0.707, only 5 patients diagnosed with double-level spondylolysis, p < 0.001), and SVA (r = 0.356, p = 0.010). However, L5I PI was found to be higher in double-level spondylolysis was shown to negatively correlate with TK (r = −0.327, p versus single-level spondylolysis (61.0° ± 10.8° vs 71.0° ± = 0.019), L4–S1 SL (r = −0.548, p < 0.001), and LDI (r = 7.7°, p = 0.037). Nevertheless, based on a large cohort of −0.724, p < 0.001). spondylolysis patients, our study found no statistically significant differences in PT when comparing the multi_lysis Quality of Life and mono_lysis groups (58.0° ± 11.9° vs 55.9° ± 11.3°, p = Regarding both functional and clinical outcomes, the 0.206). One explanation for this inconsistency may be due multi_lysis group reported worse ODI scores (mean 55.7 to the fact that the occurrence of spondylolysis in some ± 10.1 vs 44.1 ± 11.4, p < 0.001) and VAS back pain scores patients (8 of 51 multi_lysis patients with PI < 45°) might result from the “nutcracker” mechanism.6,7 In addition, (mean 6.6 ± 2.0 vs 6.0 ± 1.6, p = 0.016) than the mono_ 19 27 lysis group. No significant differences in VAS leg pain both Oh et al. and Park et al. found that the PI param- scores were observed when comparing the 2 subgroups. eter did not statistically differ between the L4–5 mono_ly- sis and L5–S1 mono_lysis groups. Here, we assumed that multi_lysis was an accidental event for more than single Discussion spondylolytic segments occurring in a single patient, who The goal of this study was to illustrate the sagittal align- had a shear stress impact on multisegmental posterior ele- ment pattern in a large cohort of patients diagnosed with ment dysplasia and/or a weak muscle-ligament-iliac com- spondylolytic spondylolisthesis, including both multi_ly- plex.7,9,28 sis and mono_lysis. We observed that patients with multi_ This study demonstrated that increased PI in multi_ly- lysis or mono_lysis exhibited abnormal pelvic morphol- sis cases was correlated with increased L5I (r = 0.745, p < ogy and orientation, insufficient LL, and forward trunk in 0.001). Similar to PI, L5I represents the orientation of the comparison with healthy controls. It is worth mentioning L5 vertebra and regulates the mechanical environment of that patients in the multi_lysis group had a significantly the lower lumbar spine. Previously, Zhu et al.24 demon- higher PT and PT/PI ratio and lower LL, L4–S1 SL, and strated that strong correlations exist between L5I and PI or LDI, which results in an increased tendency for sagittal sagittal alignment parameters in healthy individuals (r = decompensation. At the same time, L5I was detected to 0.818, p < 0.001), indicating that L5I is a crucial parameter be significantly elevated in the multi_lysis group and sig- for the lumbosacral region. Nevertheless, it was interest- nificantly correlated with PT, PT/PI, SVA, L4–S1 SL, and ing that a higher L5I in multi_lysis cases was found to be LDI. In addition, the multi_lysis group had slightly worse significantly higher than that observed in the mono_lysis ODI scores and VAS back pain scores than the mono_ly- cases, despite PI being similar between the 2 subgroups. sis group. It is possible that high L5I causes more tension at the pars In this study, there was an 11.3% incidence of multi_ly- interarticularis of supradjacent levels, where a shear stress sis in patients with spondylolytic spondylolisthesis. Ravi- mechanism7 likely results in additional spondylolysis. In chandran26 reported that 1.48% of patients with back pain brief, a higher PI was a risk factor for lumbosacral spon-

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FIG. 3. Comparison of sagittal alignment parameters between the control group and the spondylolysis group.

dylolysis (L5). A higher L5I together with a high PI could cral region, more so in the multi_lysis group than in the cause even more tension on the pars interarticularis at L5, mono_lysis group (59% ± 21% vs 64% ± 12%, p = 0.012). causing greater tension at the supradjacent level (L4) and The lack of lower LL is one of the primary causes of sagit- even at the second supradjacent level (L3), thus resulting tal malalignment.22,30 in multi_lysis. Furthermore, our work showed that sagittal malalign- To the best of our knowledge, elevated PI results in a ment in spondylolysis patients was anterior due to insuf- greater LL, which increases shear stress in the pars inter- ficient LL in lower lumbar alignment. To compensate for articularis.7,9 As shown in this study, a high PI can gener- the trunk tilting forward, compensatory mechanisms such ate high LL and L4–S1 SL in both the mono_lysis and as thoracic flattening, adjacent mobile segments in the up- multi_lysis groups. However, LDI for both the spondy- per lumbar spine, and pelvic retroversion are enhanced.6,22 lolysis subgroups was significantly lower than what was However, there is a maximum limit of compensatory observed in the healthy control group. Similar to what is mechanisms that can be achieved. For example, a signif- described in the literature, approximately two-thirds of LL icantly lower TK in the spondylolysis group than in the occurs from the L4 to S1 segments in healthy subjects.29 control group, with no statistically significant differences Findings from this study highlighted that the loss of LL between the spondylolysis subgroups, revealed a limit of in the spondylolysis group mainly occurs in the lumbosa- the thoracic flattening mechanism. It should also be high-

TABLE 3. Comparison of mean sagittal parameters among the control, multi_lysis, and mono_lysis groups p Value Control Multi_Lysis Mono_Lysis 1-Way ANOVA Multi_Lysis vs Control Mono_Lysis vs Control Multi_Lysis vs Mono_Lysis PI (°) 46.2 ± 10.1 58.0 ± 11.9 55.9 ± 11.3 <0.001 <0.001 <0.001 0.206 PT (°) 11.2 ± 6.2 19.0 ± 9.0 16.3 ± 7.6 <0.001 <0.001 <0.001 0.018 SS (°) 34.9 ± 7.6 39.1 ± 8.7 39.6 ± 8.3 <0.001 0.001 <0.001 0.679 L5I (°) 18.2 ± 9.4 30.8 ± 14.8 26.0 ± 11.2 <0.001 <0.001 <0.001 0.004 LL (°) 50.5 ± 9.9 53.4 ± 12.0 57.6 ± 10.7 <0.001 0.084 <0.001 0.005 L4–S1 SL (°) 34.8 ± 7.7 32.8 ± 13.2 37.2 ± 9.1 <0.001 0.186 0.004 0.004 TK (°) 37.2 ± 11.9 26.0 ± 11.1 28.0 ± 9.2 <0.001 <0.001 <0.001 0.157 SVA (mm) −5.3 ± 24.9 24.0 ± 39.7 1.8 ± 35.7 <0.001 <0.001 0.021 <0.001 PT/PI (%) 23 ± 11 32 ± 12 29 ± 10 <0.001 <0.001 <0.001 0.039 LDI (%) 69 ± 13 59 ± 21 64 ± 12 <0.001 <0.001 <0.001 0.012

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TABLE 4. Comparison of spinal and pelvic balance between the TABLE 5. Pearson correlations in the multi_lysis group multi_lysis group and the mono_lysis group PI L5I Multi_Lysis Mono_Lysis p Value r p Value r p Value Spinal balance, cm PT (°) 0.668 <0.001 0.860 <0.001 SVA ≥4 15 55 SS (°) 0.641 <0.001 0.165 0.247 0.003 SVA <4 36 347 L5I (°) 0.745 <0.001 0.745 <0.001 Pelvic balance LL (°) 0.337 0.016 −0.107 0.454 Low PT/high SS 23 238 L4–S1 SL (°) −0.097 0.5 −0.548 <0.001 0.039 High PT/low SS 28 164 TK (°) −0.241 0.089 −0.327 0.019 Values are presented as the number of patients unless otherwise indicated. SVA (mm) 0.247 0.08 0.356 0.01 PT/PI (%) 0.358 0.01 0.707 <0.001 LDI (%) −0.426 0.002 −0.724 <0.001 lighted that an unbalanced pelvis was observed in more patients in the multi_lysis group than in the mono_lysis group (54.9% vs 40.8%, p = 0.039) due to limitations in pelvic retroversion compensation. These limited compen- solid fusion, should be considered to correct lumbosacral satory mechanisms are insufficient to correct for anterior deformities and sagittal spinal malalignment. malalignment, leading to more cases of multi_lysis with a While there are several strengths, this study also has sagittal imbalance of the spine compared with what is seen several limitations. For one, this was a retrospective in mono_lysis cases (29.4% vs 13.7%, p = 0.003). study conducted using a single-center database, and thus Sagittal alignment is known to influence functional this work needs to be repeated in other centers with dif- and clinical reported outcomes.11 Multilevel spondylolytic ferent patient groups. Second, the natural history of the spondylolisthesis may have certain cumulative effects on multi_lysis could not be identified in patients. Next, spi- slip degrees, loss of LL, pelvic retroversion, and related nopelvic sagittal alignment at different positions was not sagittal malalignment. The global sagittal malalignment of thoroughly evaluated. Lastly, other potential confounding multi_lysis can lead to an array of symptoms that compro- factors for sagittal alignment, such as stenosis, were not mise QOL.11 High stress at the lumbosacral region results analyzed. However, this study, which described the sagit- in disc degeneration,10 additive effects of multisegmental tal malalignment in spondylolytic spondylolisthesis cases, instability, or lumbar spinal stenosis,2,10,31 which may ul- included a large proportion of patients with multi_lysis. timately lead to worse QOL outcomes in multi_lysis patients versus mono_lysis patients, including in this study. Conclusions This study has two major strengths. First, the loss of LL in the multi_lysis group, mainly occurring at the lum- There was an 11.3% incidence rate of multi_lysis in bosacral region, suggests that restoration of lordosis in the patients with symptomatic spondylolytic spondylolisthe- L4–S1 region is a priority for a lumbar surgical treatment sis observed in this study. A high-PI pattern of spino- algorithm.32 Biomechanically, the shear forces at the ad- pelvic sagittal alignment was associated with the occur- jacent segment are significantly higher in patients with rence of spondylolysis (both mono_lysis and multi_lysis), inadequate restoration of lordosis in the lower lumbar and high L5I may be associated with the development of spine.15 Inadequate restoration of lordosis in the L4–S1 re- consecutive multi_lysis. In contrast to mono_lysis cases, gion is a strong risk factor for adjacent-segment disease.32 more multi_lysis cases showed anterior global malalign- Second, patients with pelvic retroversion compensation, ment with insufficient lower LL and an unbalanced pelvis. particularly for an unbalanced pelvis, should focus on the These findings emphasize the need for an adapted surgical maintenance and the restoration of normal pelvic balance correction in spondylolysis patients with distinct sagittal through lumbar reconstructive procedures. Hresko et al.23 spinal malalignment, particularly in those exhibiting the suggested that surgical reduction might be considered characteristics of multi_lysis. for patients exhibiting an unbalanced pelvis. Alzakri and colleagues33 further demonstrated that achieving normal Acknowledgments pelvic balance postoperatively in high-grade spondylolis- This work was supported by the National Natural Science thesis cases was associated with better improvement in Foundation of China (grant no. 81772422) and the Natural Science QOL. As demonstrated in the novel global alignment and Foundation of Jiangsu Province (BE2017606 and BK20170126). proportion score,12 spinopelvic malalignment of unharmo- nious LDI and relative pelvic version in the spondyloly- References sis group should be aligned in lumbar fusion surgery to reduce mechanical complication rates and improve long- 1. Fredrickson BE, Baker D, McHolick WJ, et al. The natural 13 history of spondylolysis and spondylolisthesis. J Bone Joint term QOL. Based on our data, surgical strategies, such as Surg Am. 1984;66(5):699–707. release of the surrounding soft tissue to increase the rate of 2. He LC, Wang YX, Gong JS, et al. Prevalence and risk fac- slip reduction, inserting a cage to restore the height of the tors of lumbar spondylolisthesis in elderly Chinese men and intervertebral space, and insertion of a full bone graft for women. Eur Radiol. 2014;24(2):441–448.

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Twenty-nine-year follow- Conception and design: Sun, Zhou, Wang, Qiu. Acquisition of up of nonoperatively treated three-level lumbar spondyloly- data: Sun, Zhou, Qian, Zhu, Wang, Qiu. Analysis and interpreta- sis: a case report and review of the literature. JBJS Case tion of data: Sun, Zhou, Xu, Qiu. Drafting the article: Sun, Zhou, Connect. 2016;6(1):e13. Qiu. Critically revising the article: Sun, Zhou, Chen, Qian, Zhu, 18. Wáng YXJ, Deng M, Griffith JF, et al. Lumbar spondylolis- Wang. Reviewed submitted version of manuscript: Sun, Zhou, Xu, thesis progression and de novo spondylolisthesis in elderly Qian, Zhu, Wang. Approved the final version of the manuscript Chinese men and women: a year-4 follow-up study. Spine on behalf of all authors: Sun. Statistical analysis: Sun, Zhou, Xu. (Phila Pa 1976). 2016;41(13):1096–1103. Administrative/technical/material support: Sun, Zhou. Study 19. Oh SK, Chung SS, Lee CS. Correlation of pelvic parameters supervision: Sun, Zhou, Chen, Qian. with isthmic spondylolisthesis. Asian Spine J. 2009;3(1):21– 26. Correspondence 20. Duval-Beaupère G, Schmidt C, Cosson P. A barycentremetric Xu Sun: Drum Tower Hospital, Clinical College of Nanjing Medi- study of the sagittal shape of spine and pelvis: the conditions cal University, Nanjing, China. [email protected]. required for an economic standing position. Ann Biomed Eng. 1992;20(4):451–462.

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